Early Canid Domestication: The Farm-Fox Experiment

What might have caused these changes in the fox population? Before
discussing Belyaev's explanation, we should consider other
possibilities. Might rates and patterns of changes observed in foxes
be due, for example, to inbreeding? That could be true if enough
foxes in Belyaev's founding population carried a recessive mutant
gene from the trait along with a dominant normal gene that masked
its effects. Such mixed-gene, or heterozygous, foxes would
have been hidden carriers, unaffected by the mutation themselves but
capable of passing it on to later generations.

As Morey pointed out, inbreeding might well have been rampant during
the early steps of dog domestication. But it certainly cannot
explain the novel traits we have observed in our foxes, for two
reasons. First, we designed the mating system for our experimental
fox population to prevent it. Through outbreeding with foxes from
commercial fox farms and other standard methods, we have kept the
inbreeding coefficients for our fox population between 0.02 and
0.07. That means that whenever a fox pup with a novel trait has been
born into the herd, the probability that it acquired the trait
through inbreeding (that is, by inheriting both of its mutant genes
from the same ancestor) has varied between only 2 and 7 percent.
Second, some of the new traits are not recessive: They are
controlled by dominant or incompletely dominant genes. Any fox with
one of those genes would have shown its effects; there could have
been no "hidden carriers" in the original population.

Another, subtler possibility
is that the novelties in our domesticated population are classic
by-products of strong selection for a quantitative trait. In
genetics, quantitative traits are characteristics that can vary over
a range of possibilities; unlike Gregor Mendel's peas, which were
either smooth or wrinkly with no middle ground, quantitative traits
such as an animal's size, the amount of milk it produces or its
overall friendliness toward human beings can be high, low or
anywhere in between. What makes selecting for quantitative traits so
perilous is that they (or at least the part of them that is genetic)
tend to be controlled not by single genes but by complex systems of
genes, known as polygenes. Because polygenes are so
intricate, anything that tampers with them runs the risk of
upsetting other parts of an organism's genetic machinery. In the
case of our foxes, a breeding program that alters a polygene might
upset the genetic balance in some animals, causing them to show
unusual new traits, most of them harmful to the fox. Note that in
this argument, it does not matter whether the trait being selected
for is tameness or some other quantitative trait. Any breeding
program that affects a polygene might have similar effects.

The problem with that explanation is that it does not explain why we
see the particular mutations we do see. If disrupted polygenes are
responsible, then the effects of a selection experiment ought to
depend strongly on which mutations already existed in the
population. If Belyaev had started with 130 foxes from, say, North
America, then their descendants today would have ended up with a
completely different set of novelties. Domesticating a population of
wolves, or pigs, or cattle ought to produce novel traits more
different still. Yet as Belyaev pointed out, when we look at the
changes in other domesticated animals, the most striking things
about them are not how diverse they are, but how similar. Different
animals, domesticated by different people at different times in
different parts of the world, appear to have passed through the same
morphological and physiological evolutionary pathways. How can that be?

According to Belyaev, the
answer is not that domestication selects for a quantitative
trait but that it selects for a behavioral one. He
considered genetic transformations of behavior to be the key factor
entraining other genetic events. Many of the polygenes determining
behavior may be regulatory, engaged in stabilizing an organism's
early development, or ontogenesis. Ontogenesis is an
extremely delicate process. In principle, even slight shifts in the
sequence of events could throw it into chaos. Thus the genes that
orchestrate those events and keep them on track have a powerful role
to play. Which genes are they? Although numerous genes interact to
stabilize an organism's development, the lead role belongs to the
genes that control the functioning of the neural and endocrine
systems. Yet those same genes also govern the systems that control
an animal's behavior, including its friendliness or hostility toward
human beings. So, in principle, selecting animals for behavioral
traits can fundamentally alter the development of an organism.

As our breeding program has progressed, we have indeed observed
changes in some of the animals' neurochemical and neurohormonal
mechanisms. For example, we have measured a steady drop in the
hormone-producing activity of the foxes' adrenal glands. Among
several other roles in the body, the adrenal cortex comes into play
when an animal has to adapt to stress. It releases hormones such as
corticosteroids, which stimulate the body to extract energy from its
reserves of fats and proteins.

After 12 generations of selective breeding, the basal levels of
corticosteroids in the blood plasma of our domesticated foxes had
dropped to slightly more than half the level in a control group.
After 28 to 30 generations of selection, the level had halved again.
The adrenal cortex in our foxes also responds less sharply when the
foxes are subjected to emotional stress. Selection has even affected
the neurochemistry of our foxes' brains. Changes have taken place in
the serotonin system, thought to be the leading mediator inhibiting
animals' aggressive behavior. Compared with a control group, the
brains of our domesticated foxes contain higher levels of serotonin;
of its major metabolite, 5-oxyindolacetic acid; and of tryptophan
hydroxylase, the key enzyme of serotonin synthesis. Serotonin, like
other neurotransmitters, is critically involved in shaping an
animal's development from its earliest stages.